Skip to main content
SpringerLink
Log in

Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis on different macroalgae

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Settlement of mussels is commonly associated with macroalgae. The effects of 19 macroalgal species on the settlement and metamorphosis of pediveliger larvae of the mussel Mytilus galloprovincialis were investigated in the laboratory. Settlement and metamorphosis inducing activities of macroalgae Chlorodesmis fastigiata and Ceramium tenerrimum collected each month during the period between January 2005 and April 2006 were also investigated. Furthermore, C. fastigiata and C. tenerrimum were subjected to various treatments to investigate the roles of bacteria and diatoms on the algal surface in the induction of larval settlement and metamorphosis of M. galloprovincialis and the characteristics of the cues in these two macroalgae. Pediveliger larvae of M. galloprovincialis settled and metamorphosed in high percentages on Cladophora sp., Chlorodesmis fastigiata, Centroceras clavulatum, and Ceramium tenerrimum, all of which were filamentous in morphology. Macroalgae that were cylindrical, phylloid, flabellate, palmate and pinnate all showed low (<8%) percentages of post-larvae but four other filamentous macroalgae also had low mussel larval settlement, suggesting that chemical factors may also be involved. Seasonal variation had no effect on inductive activities of C. fastigiata and C. tenerrimum. Treatment of C. fastigiata and C. tenerrimum with formalin, ethanol and heat resulted in the significant decrease or loss of their inductive activities. Survival of algal cells within treated macroalgae also decreased significantly. Treatment of the two macroalgae with antibiotics and GeO2 reduced the numbers of bacteria and diatoms on their surface but did not affect their inductive activities, indicating that the cue was produced by macroalgae and not by coexisting bacteria and diatoms. However, conditioned water and crude extracts of these two macroalgae did not induce larval settlement and metamorphosis. Thus, larvae of M. galloprovincialis settled and metamorphosed on specific filamentous macroalgae. The chemical cues produced by C. fastigiata and C. tenerrimum were susceptible to ethanol and heat treatments and were not recovered in the conditioned water nor in the extracts. The finding that inactive C. tenerrimum can be produced from culturing its apical segments provides a new tool to elucidate the chemical cue(s) from macroalgae through manipulation of their culture conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alfaro AC (2005) Effect of water flow and oxygen concentration on early settlement of the New Zealand green-lipped mussel, Perna canaliculus. Aquaculture 246:285–294

    Article  Google Scholar 

  • Alfaro AC (2006) Byssal attachment of juvenile mussels, Perna canaliculus, affected by water motion and air bubbles. Aquaculture 255:357–361

    Article  Google Scholar 

  • Alfaro AC, Copp BR, Appleton DR, Kelly S, Jeffs AG (2006) Chemical cues promote settlement in larvae of the green-lipped mussel, Perna canaliculus. Aquacult Int 14:405–412

    Article  CAS  Google Scholar 

  • Alfaro AC, Jeffs AG (2002) Small-scale mussel settlement patterns within morphologically distinct substrata at Ninety Mile Beach, northern New Zealand. Malacologia 44:1–15

    Google Scholar 

  • Alfaro AC, Jeffs AG, Creese RG (2004) Bottom-drifting algal/mussel spat associations along a sanday coastal region in northern New Zealand. Aquaculture 241:269–290

    Article  Google Scholar 

  • Bao WY, Satuito CG, Yang JL, Kitamura H (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Mar Biol 150:565–574

    Article  Google Scholar 

  • Bayne BL (1964) Primary and secondary settlement in Mytilus edulis L. (Mollusca). J Anim Ecol 33:513–523

    Article  Google Scholar 

  • Bayne BL (1965) Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia 2:1–47

    Google Scholar 

  • Bulleri F, Airoldi L, Branca GM, Abbiati M (2006) Positive effects of the introduced green alga, Codium fragile ssp. tomentosoides, on recruitment and survival of mussels. Mar Biol 148:1213–1220

    Article  Google Scholar 

  • Cáceres-Martínez J, Robledo JAF, Figueras A (1993) Settlement of mussels Mytilus galloprovinvialis on an exposed rocky shore in Ría de Vigo, NW Spain. Mar Ecol Prog Ser 93:195–198

    Article  Google Scholar 

  • Cáceres-Martínez J, Robledo JAF, Figueras A (1994) Settlement and post-larve behaviour of Mytilus galloprovinvialis: field and laboratory experiments. Mar Ecol Prog Ser 112:107–117

    Article  Google Scholar 

  • Cooper K (1981) A model to explain the induction of settlement and metamorphosis of planktonic eyed-pediveligers of the blue mussel Mytilus edulis L. by chemical and tactile cues (Abstract). J Shellfish Res 2:117

    Google Scholar 

  • Daume S, Krsinich A, Farrell S, Gervis M (2000) Settlement, early growth and survival of Haliotis rubra in response to different algal species. J Appl Phycol 12:479–488

    Article  Google Scholar 

  • Davis AR, Moreno CA (1995) Selection of substrata by juvenile Choromytilus chorus (Mytilidae): are chemical cues important? J Exp Mar Biol Ecol 191:167–180

    Article  Google Scholar 

  • Dobretsov SV (1999) Effects of macroalgae and biofilm on settlement of blue mussel (Mytilus edulis L.) larvae. Biofouling 14:153–165

    Article  Google Scholar 

  • Dobretsov SV, Railkin AI (1994) Correlative relationships between marine microfouling and macrofouling. Russ J Mar Biol 20:87–90

    Google Scholar 

  • Eyster LS, Pechenik JA (1987) Attachment of Mytilus edulis L. larvae on algal and byssal filaments is enhanced by water agitation. J Exp Mar Biol Ecol 114:99–110

    Article  Google Scholar 

  • Hadfield MG, Paul VG (2001) Natural chemical cues for settlement and metamorphosis of marine-invertebrate larvae. In: McClintock JB, Baker JB (eds) Marine chemical ecology. CRC, Boca Raton, pp 431–461

    Google Scholar 

  • Harder T, Dobretsov S, Qian PY (2004) Waterborne polar macromolecules act as algal antifouling in the seaweed Ulva reticulate. Mar Ecol Prog Ser 274:133–141

    Article  CAS  Google Scholar 

  • Huggett MJ, de Nys R, Williamson JE, Heasman M, Steinberg PD (2005) Settlement of larval blacklip abalone, Haliotis rubra, in response to green and red macroalgae. Mar Biol 147:1155–1163

    Article  Google Scholar 

  • Huggett MJ, Williamson JE, de Nys R, Kjelleberg S, Steinberg PD (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619

    Article  PubMed  Google Scholar 

  • Iwasaki H (1961) The life-cycle of Porphyra tenera in vitro. Biol Bull 121:173–187

    Article  Google Scholar 

  • Johnson CR, Sutton DC (1994) Bacteria on the surface of crustose coralline algae induce metamorphosis of the crown-of-thorns starfish Acanthaster planci. Mar Biol 120:305–310

    Article  Google Scholar 

  • Kajihara T (1985) The mussel Mytilus galloprovincialis—the valiant invader of coastal sea area. In: Okiyama M, Suzuki K (eds) Japanese marine organisms—Ecology of invasion and disturbance (Nihon no kaiyo seibutsu shinryaku to kakuran noseitaigaku, In Japanese). Tokai University Press, Tokyo, pp 49–54

    Google Scholar 

  • Kajihara T, Oka M (1980) Seasonal occurrence of marine mussel plantigrades in Tokyo Harbor. Bull Jpn Soc Sci Fish 46:145–148

    Google Scholar 

  • Katsuyama I (1995) Filamentous organisms observed with the blue mussel. Marine Fouling 11:9–13

    Article  Google Scholar 

  • Kirchman D, Graham S, Reish D, Mitchell R (1982) Bacteria induce settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). J Exp Mar Biol Ecol 56:153–163

    Article  Google Scholar 

  • Kitamura H, Kitahara S, Koh HB (1993) The induction of larval settlement and metamorphosis of two sea urchins, Pseudocentrotus depressus and Anthocidaris crassispina, by free fatty acids extracted from the coralline red alga Corallina pilulifera. Mar Biol 115:387–392

    Article  CAS  Google Scholar 

  • Krug PJ, Manzi AE (1999) Waterborne and surface-associated carbohydrates as settlement cues for larvae of the specialist marine Herbivore Alderia modesta. Biol Bull 197:94–103

    Article  CAS  Google Scholar 

  • Lau SCK, Qian PY (2001) Larval settlement in the serpulid polychaete Hydroides elegans in response to bacterial films: an investigation of the nature putative larval settlement cue. Mar Biol 138:321–328

    Article  Google Scholar 

  • Li JY, Rahim SAKA, Satuito CG, Kitamura H (2004a) Combination of macroalgae-conditionded water and periphytic diatom Navicula ramosissima as an inducer of larval metamorphosis in the sea urchins Anthocidaris crassispina and Pseudocentrotus depressus. Sessile Organisms 21:1–6

    Google Scholar 

  • Li JY, Rahim SAKA, Satuito CG, Kitamura H (2004b) Characterization of the active substances in water conditioned by the coralline red alga Corallina pilulifera as inducers of metamorphosis in larvae of the sea urchin Anthocidaris crassispina (in Japanese with English abstract). Sessile Organisms 21:41–46

    CAS  Google Scholar 

  • McGrath D, King PA, Gosling EM (1988) Evidence for the direct settlement of Mytilus edulis larvae on adult mussel beds. Mar Ecol Prog Ser 47:103–106

    Article  Google Scholar 

  • Moreno CA (1995) Macroalgae as a refuge from predation for recruits of the mussel Choromytilus chorus (Molina, 1782) in Southern Chile. J Exp Mar Biol Ecol 191:181–193

    Article  Google Scholar 

  • Morse ANC, Morse DE (1984) Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surfaces of crustose red algae. J Exp Mar Biol Ecol 75:191–215

    Article  CAS  Google Scholar 

  • Pearce CM, Scheibling RE (1991) Effect of macroalgae, microbial films, and conspecifics on the induction of metamorphosis of the green sea urchin Strongylocentrotus droebachiensis (Müller). J Exp Biol Ecol 147:147–162

    Article  Google Scholar 

  • Petersen JH (1984) Larval settlement behavior in competing species: Mytilus californianus Conrad and M. edulis L. J Exp Mar Biol Ecol 82:147–159

    Article  Google Scholar 

  • Ramírez SC, Cáceres-Martínez J (1999) Settlement of blue mussel Mytilus galloprovincialis Lamarck on artificial substrates in Bahía De Todos Santos B.C., México. J shellfish Res 18:33–39

    Google Scholar 

  • Sakaguchi I (1987) Bivavles. In: Kajihara T (ed) Attaching organisms and aquaculture (in Japanese). Kouse Press, Tokyo, pp 100–107

    Google Scholar 

  • Sakaguchi I (2003) A review of antifouling technologies in power plant cooling water systems (in Japanese with English abstract). Sessile Organisms 20:15–19

    Google Scholar 

  • Sakaguchi I, Kajihara T (1988) Recruitment from larvae to fouling community of marine mussel (in Japanese with English abstract). Marine Fouling 7:23–29

    Article  Google Scholar 

  • Satuito CG, Bao WY, Yang JL, Kitamura H (2005) Survival, growth, settlement and metamorphosis of refrigerated larvae of the mussel Mytilus galloprovincialis Lamarck and their use in settlement and antifouling bioassays. Biofouling 21:217–225

    Article  PubMed  Google Scholar 

  • Satuito CG, Natoyama K, Yamazaki M, Fusetani N (1995) Induction of attachment and mtamorphosis of laboratory cultured mussel Mytilus edulis galloprovincialis larvae by microbial film. Fish Sci 61:223–227

    CAS  Google Scholar 

  • Satuito CG, Shimizu K, Fusetani N (1997) Studies on the factors influencing larval settlement in Balanus amphitrite and Mytilus galloprovincialis. Hydrobiologia 358:275–280

    Article  Google Scholar 

  • Schmitt TM, Lindquist N, Hay ME (1998) Seaweed secondary metabolites as antifoulants: effects of Dictyota spp. diterpenes on survivorship, settlement, and development of marine invertebrate larvae. Chemoecology 8:125–131

    Article  CAS  Google Scholar 

  • Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on the exposed rocky shores. I. breeding and settlement. Oecologia (Berlin) 3:277–316

    Article  Google Scholar 

  • Swanson RL, Williamson JE, de Nys R, Kumar N, Bucknall MP, Steinberg PD (2004) Induction of settlement of larvae of the sea urchin Holopneustes purpurascens by histamine from a host alga. Biol Bull 206:161–172

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Itoh K, Ishii M, Suzuki M, Itabashi Y (2002) Induction of larval settlement and metamorphosis of the sea urchin Strongylocentrotus intermedius by glycoglycerolipids from the green alga Ulvella lens. Mar Biol 140:763–771

    Article  CAS  Google Scholar 

  • Tatewaki M (1992) Isolation and culture of macroalgae. In: Nisizawa K, Tihara M (eds) Methods in phycological studies (in Japanese). Kyouritu Press, Tokyo, pp 53–106

    Google Scholar 

  • Unabia CRC, Hadfield MG (1999) Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar Biol 133:55–64

    Article  Google Scholar 

  • Walters LJ, Hadfield MG, Smith CM (1996) Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement. Mar Biol 126:383–393

    Article  Google Scholar 

  • Yvin JC, Chevolot L, Chevolot-Magueur AM, Cochard JC (1985) First isolation of jacaranone from an alga, Delesseria sanguinea. A metamorphosis inducer of Pectin larvae. J Nat Prod 48:814–816

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Nagasaki Prefectural Institute of Fisheries for their cooperation in the collection of adult mussels and macroalgae. The authors are also grateful to Dr. K. Kuwano (Nagasaki University) for identification of macroalgae and to Mr. M. Hirano for technical assistance. All experiments complied with the current Japanese laws.

Author information

Authors and Affiliations

  1. Graduate School of Science and Technology, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki-shi, 852-8521, Nagasaki, Japan

    Jin-Long Yang, Cyril Glenn Satuito & Wei-Yang Bao

  2. Faculty of Fisheries, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki-shi, 852-8521, Nagasaki, Japan

    Hitoshi Kitamura

Authors
  1. Jin-Long Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cyril Glenn Satuito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei-Yang Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hitoshi Kitamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jin-Long Yang.

Additional information

Communicated by S. Nishida.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, JL., Satuito, C.G., Bao, WY. et al. Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis on different macroalgae. Mar Biol 152, 1121–1132 (2007). https://doi.org/10.1007/s00227-007-0759-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0759-0

Keywords

Search

Navigation